Reviewed Article
Folia Primatol 2004;75:295–316
DOI: 10.1159/000080208
Received: May 14, 2003
Accepted after revision: January 15, 2004
Nigerian Chimpanzees (Pan troglodytes
vellerosus) at Gashaka:
Two Years of Habituation Efforts
Volker Sommera
Andrew Fowler a
Jeremiah Adanub
Isabelle Faucher a
a
Department of Anthropology, University College London, London, UK;
Department of Forestry and Wildlife Management, Federal University of
Technology, Yola, Nigeria
b
Key Words
Nigerian chimpanzee ` Habituation ` Call pattern ` Party size
Abstract
Cross-population comparisons of chimpanzees can shed light on the pathways of hominid evolution. So far, no eco-ethological data exist for the recently
recognized subspecies Pan troglodytes vellerosus. We report on the first 2 years
of a new long-term study from what is perhaps their last remaining stronghold:
the Gashaka Gumti National Park, Nigeria. The mosaic habitat (woodland, lowland and gallery forest) receives 1,826 mm rain/year, with 4–5 months being
completely dry. Primates at Gashaka are not hunted, and the chimpanzees are
therefore relatively tolerant of human observers. We focused on the GashakaKwano community, investing 3,000 h of patrols. A total of 95 sightings were
achieved which lasted for an average of 27 min (range 1–190 min). Party size
averaged 3.7 animals (range 1–17) but was, similarly to encounter length, susceptible to a wide range of methodological, social and ecological factors. The
Kwano community comprises at least 35 members which occupy a home range
of at least 26 km 2, yielding a density of 1.3/km2. The area represents the West
African equivalent of a chimpanzee site similar to the forest-woodland habitat in
which early humans might have evolved.
Copyright © 2004 S. Karger AG, Basel
Ó2004 S. Karger AG, Basel
0015–5713/04/0755–0295$21.00/0
Fax + 41 61 306 12 34
E-Mail karger@karger.ch
www.karger.com
Accessible online at:
www.karger.com/fpr
V. Sommer, Department of Anthropology
University College London, Gower Street
London WC1E 6BT (UK)
Tel. +44 20 7679 7030, Fax +44 20 7679 7728
E-Mail v.sommer@ucl.ac.uk
Introduction
Chimpanzees (Pan troglodytes) have been studied across Africa since the
1960s [reviews in Goodall, 1986; Wrangham et al., 1994; Boesch and BoeschAchermann, 2000; Boesch et al., 2002]. Attempts to reconstruct the probable behavioural suite of the last common ancestor of apes and humans [Moore, 1996]
found that both chimpanzee and human societies exhibit tool use, hunting, territorial aggression, war-like raiding and cultural differences which are inexplicable by
ecological variables [Manson et al., 1991; McGrew, 1992; Whiten et al., 1999].
Chimpanzees [for the following, see reviews in Goodall, 1986; Boesch and
Boesch-Achermann, 2000; Boesch et al., 2002] are agile arborealists, but can also
knuckle-walk rapidly on the ground. Their omnivorous diet consists primarily of
fruit and plant parts, but includes insects and various mammals such as monkeys,
duikers and bush pigs. Chimpanzees live in large multi-male/multi-female groups,
so-called communities, of typically 30–80 members. Chimpanzee social life is
characterized by fusion-fission in that the larger community separates daily into
smaller parties which travel, forage, rest and nest together. Parties communicate by
vocalizing and drumming. Numerous ecological (e.g. food distribution, rainfall),
social (e.g. oestrous females or infants present) and spatial factors (e.g. location
within the home range) correlate with party size. Nevertheless, the underlying
causes are often obscure, and party sizes vary considerably between sites.
Understanding the flexibility in chimpanzee behaviour and ecology requires
data from diverse ecological locations [Wrangham et al., 1994; Whiten et al.,
1999]. However, relatively few long-term studies exist, and sites where chimpanzees are habituated to human observers are even rarer. Moreover, wild chimpanzees
are increasingly driven into local extinction due to habitat destruction and hunting
[Pearce and Ammann, 1995; Sommer and Ammann, 1998].
Recently, based on genetic analyses from hair samples, a fourth chimpanzee
subspecies has been recognized: Pan troglodytes vellerosus, the Nigerian chimpanzee [Gonder et al., 1997], distributed between the confluence of the Benue and Niger in Nigeria and the Sanaga river in Cameroon. However, the apes have already
been displaced from most of these areas by human activity. Detailed data on their
behaviour or ecology are lacking. Several mostly unpublished reports describe distribution and nest-building activity in what is perhaps the last remaining stronghold
of P. t. vellerosus, the Gashaka area in Nigeria [Dunn, 1993; Harcourt and Ellerton,
1995; Hogarth, 1997; Adanu, 1997, 1998; Foster, 1998; Lameed, 2002].
Our paper reports on the first 2 years (2000–2001) of a new long-term study at
Gashaka, providing details about acoustic signals, party size and the progress of
habituation efforts. This supplements knowledge about other subspecies and will
hopefully improve the understanding of chimpanzee and human evolution.
Material and Methods
The Gashaka Primate Project
The Gashaka Gumti National Park (GGNP) lies in Eastern Nigeria on the border with
Cameroon (06°55’–08°13’ N and 11°13’–12°11’ E; fig. 1). GGNP was gazetted from two
game reserves in 1991 and is, with about 6,500 km2, Nigeria’s largest national park (for the
296
Folia Primatol 2004;75:295–316
Sommer/Adanu/Faucher/Fowler
Fig. 1. Location of GGNP/Nigeria (courtesy Y. Warren).
following, see Dunn [1999]). Human population in the park has declined over the last decade, due to relocation and migration towards more easily accessible areas.
The southern (Gashaka) sector of the park has rugged terrain from about 300 m up to
2,419 m at Chappal Waddi (Gangirwal), Nigeria’s highest mountain. It is an important water
catchment area for the Benue river. Abundant rivers flow continuously, even throughout the
markedly dry season. The park area around the village of Gashaka in southern Taraba state
harbours a great diversity of wildlife, including 6 species of diurnal primates. It is probably
the only region where a sizable population of P. t. vellerosus has a long-term prospect of
survival.
The Gashaka Primate Project was established in 1999 with the aims of (a) understanding how environmental factors influence the structure of primate societies and (b) contributing to primate conservation. The Gashaka Primate Project works with students and researchers from Africa and western countries and is logistically supported by GGNP and the Nigerian Conservation Foundation.
A research station is available in Gashaka (elevation 320 m), a village of about 600
people on the edge of the park. The major study site is inside the park at Kwano (583 m;
07°19’ N, 11°35’ E), an abandoned settlement, 10.5 aerial km from Gashaka. A field station
Nigerian Chimpanzees at Gashaka
Folia Primatol 2004;75:295–316
297
Fig. 2. Climate during the 2000/2001 study period. Recorded by Nigerian Conservation
Foundation weather station in Gashaka village (elevation 320 m). Humidity measured at
16.00 h.
was erected at Kwano in 2001. An ancient footpath connects Gashaka with Kwano, leading
to the highlands and on to Cameroon. The path (traffic approx. 1 person/h) was widened in
1999 so that vehicles can reach Kwano during the dry season. However, during rains, a walk
of about 3 h provides the only access. Serti, the nearest town and site of GGNP headquarters,
is 40 km away. Vehicles connect Serti and Gashaka during the dry season, but the wet season requires precarious river crossings with canoes.
Conservation Status
The Gashaka-Kwano area is not a pristine forest but experienced anthropogenic influence throughout centuries. Most notable is the deliberate yearly burning of grass (from December to January) by locals and park authorities which likely turned large parts of previous
semi-deciduous forest into grassy woodland [Louppe et al., 1995]. Large-scale logging does
not exist, although some timber and non-timber forest products are extracted. From time to
time, Fulani pastoralists will graze cattle. All hunting is prohibited in GGNP although ungulates and pigs are illegally hunted. However, during 4 years of study at Kwano (1999–2003),
we did not find any snare although they are occasionally encountered around Gashaka. One
adult female chimpanzee is known to be missing a hand; she was probably accidentally
caught in a snare. Monkeys or chimpanzees are not hunted in the Gashaka-Kwano region,
because of religious taboos connected with Islam. Primates will not react discernibly if a gun
is pointed at them, indicating that they have not been hunted for a long time. These taboos
do not extend to crop-raiding baboons or tantalus monkeys near villages who are sometimes
shot or poisoned [Dunn, 1993; pers. observation]. Primates are poached in other parts of the
park – particularly near the Cameroonian border –, typically as part of a trade in bushmeat
by non-indigenous hunters. Nevertheless, Gashaka-Kwano is an area with considerable conservation potential, particularly for non-human primates.
Climate
Weather data were recorded at Gashaka village. Average temperatures should be about
3°C less at Kwano, given the higher altitude. The climate fluctuates half-yearly between
a dry and a wet season (fig. 2). Rains may start in mid March. The average number of
rainy days per month during the heavy downpours from mid April to mid October was 18
298
Folia Primatol 2004;75:295–316
Sommer/Adanu/Faucher/Fowler
Fig. 3. Woodland savannah and lowland tropical rain forest cover the undulating hills in
the Gashaka-Kwano area (photo: V. Sommer).
(range 11–22). The wettest day (August 2001) saw 144 mm rain. The yearly average reached
1,826 mm (year 2000: 1,875 mm during 127 rainy days; year 2001: 1,777 mm during 124
days). No rain falls during at least 4 months/year (November–February). The mean monthly
humidity (at 16.00 h) had a minimum of 15% (February 2001) and a maximum of 78%
(September 2001). The dry season coincides with the Harmattan period (November–March),
when a dry dusty wind blows from the Sahara. The mean minimum temperature was 21°C,
the coolest day 13°C (January 2001), the mean maximum temperature 33°C, and the hottest
day 41°C (March 2000).
Flora
The Gashaka-Kwano area is located in the sub-Saharan Guinea zone, representing a
mosaic of habitats. Montane forests, open (montane) grassland and swamps can be found
outside the study area; the Kwano region itself is characterized by woodland, lowland and
gallery forest (fig. 3) [for details, see Dunn, 1999; Chapman and Chapman, 2001].
Woodland – also known as Guinea savannah – is dominated by a ground cover of
coarse grasses 2–3 m high (e.g. Andropogon spp., Hyparrhenia spp.). Trees are relatively
small, dispersed and often fire-resistant, including Lophira lanceolata, Daniellia oliveri,
Afzelia africana, Crossopteryx febrifuga, Piliostigma thonningii, Entada africana, Prosopis
africana, Annona senegalensis, Combretum spp., Terminalia spp., Parkia biglobosa.
Families most commonly found in the often stratified lowland forest include Leguminosae, Sterculiaceae, Apocynaceae and Moraceae. Emergents may grow up to 40 m high and
include Khaya grandifolia, Milicia excelsa as well as trees with characteristic buttress roots
such as Terminalia superba or Ceiba pentandra. At 15–35 m, species such as Trilepisium
Nigerian Chimpanzees at Gashaka
Folia Primatol 2004;75:295–316
299
madagascariense, Pseudospondias preussi and Afzelia spp. may form a closed canopy. Trees
found in the next lower storey include Celtis zenkeri, Albizia spp., Erythrophleum
suaveolens, Campylospermum spp. and Psydrax spp. Below grow small trees of 2–8 m and
shrubs like Cnestis ferruginea, Connarus griffonianus, Psychotria peduncularis, Celtis
philippensis, Campylospermum flavum, Psydrax subcordata, Monodora tenuifolia and Olax
subscorpoidea. The forest floor may be covered by a herbaceous layer and mosses, ferns and
orchids. Lianas and epiphytes are abundant throughout the forest.
Gallery forest along muddy stream banks includes Pandanus candelabrum and Costus
spp., while those along rivers and streams contain Brachystegia eurycoma, Berlinia grandiflora, E. suaveolens, Blighia unijugata and Phoenix reclinata.
Fauna
The Gashaka-Kwano habitat supports a wide variety of large animals (table 1), particularly mammals, including 6 diurnal species of non-human primates. Potential predators of
primates include leopards and monkey-hunting raptors such as the crowned eagle
(Stephanoaetus coronatus). Ungulates are not abundant because of past rinderpest epidemics
[Dunn, 1999] and poaching.
Methodology
Patrol teams traversed the Kwano area from 6.00 to 18.00 h to gather information about
chimpanzees during 111 days in the year 2000 and during 247 days in the year 2001. Patrols
covered 23/24 study months (table 2). The combined recording time for 2000 was 678 h,
whereas 2,316 h were invested in 2001, yielding a total of 2,994 h.
Patrols were scheduled to cover 12 h of a given day (6.00–6.59, 7.00–7.59,.... 16.00–
16.59, 17.00–17.59 h). We obtained records for 269 (97.4%) of the 23 × 12 = 276 individual
hours of days.
The number of patrols was 515. The number of persons in a given patrol – students,
researchers, local field assistants, volunteers – could vary (1 = 19.6%, 2 = 53.8%, 3 =
18.1%, 4 = 6.4%, 5 = 1.2%, 6 = 0.6%, >6 = 0.4%).
The patrols walked paths and specially cut trails or sat at elevated observation points.
They recorded time and location of any chimpanzee vocalization (typically pant-hoots, barks
or screams) and drumming of buttress roots or tree boles [Goodall, 1986].
The patrols used auditory contact or recently constructed chimpanzee nests to find the
apes. They were instructed (a) not to approach further when they saw chimpanzees, (b) not to
hide upon visual contact but to make their approach known to the apes, e.g. by talking in a
quiet voice, and (c) to mock-chew vegetation once visible to the apes to convey nonaggressive intentions. The Gashaka-Kwano chimpanzees would often tolerate human observers and at other times retreat more or less quickly. The patrols remained near the chimpanzees
until they changed location. To follow the apes in the rugged terrain was not normally possible. Researchers or labourers would also meet chimpanzees by coincidence, usually near the
footpath. Information about these opportunistic encounters was included in the analysis.
Acoustic signals (vocalization, drumming) were analysed in a one-zero fashion, employing 1-min intervals. Rates were calculated for each hour of the day for each given
month. For example, a total of 1,680 min (28.0 h) of patrols fell into the period from 10.00
to 10.59 h in April 2001 when acoustic signals were recorded during 25 min, yielding a rate
of 0.89/h. The mean hourly values were summed up and averaged, resulting in a mean
hourly score per month.
Acoustic signals are often repetitive, occurring in ‘bouts’. Such bouts are not clustered
in an obviously discrete pattern, i.e. it is ambiguous when they begin and end. We defined
bouts through a statistical criterion [Martin and Bateson, 1986]. An individual signal was
defined as lasting as long as successive one-zero 1-min intervals had an entry. A bout criterion interval can then be derived from a frequency histogram of intervals between signals
(no entry for up to 1 min, up to 2 min, 3 min etc.). From this, a graph is developed where the
X-axis represents interval length (min) and a logged Y-axis the cumulative percent of individual intervals (1 min, 2 min, 3 min...). The resulting log survivorship curve is expected to
300
Folia Primatol 2004;75:295–316
Sommer/Adanu/Faucher/Fowler
Table 1. Large animals in the Gashaka-Kwano chimpanzee home range region (2000–2001)
Taxon
Common name
Latin name
Hausa name
Sightings1
Primates
Chimpanzee
Pan troglodytes
vellerosus
Papio anubis
Cercopithecus nictitans
Biri mai ganga
see text
Gogo
Bakinbiri
C
C
Gimchiki
Kirikaa
Biri mai roro
Pangolins
Rodents
Carnivores
Baboon
Putty-nosed
monkey
Mona monkey
Tantalus monkey
Guereza
Galago
Tree pangolin
Derby's flying
squirrel
Gambian sun
squirrel
Brush-tailed
porcupine
Crested porcupine
Gambian giant rat
Spot-necked otter
African civet
Leopard
Golden cat
Wild dog2
Lion2
Spotted hyaena
Aardvarks
Ungulates
Reptiles
Birds
2
Aardvark
Rock hyrax
Red river hog
Warthog
Cercopithecus mona
Cercopithecus aethiops
Colobus guereza
Galago spp.?
Phataginus tricuspis
Anomalurus derbianus
Dankunya
Kurege
C
O
C
R
R
R
Heliosciurus gambianus
Kurege
C
Atherurus africanus
Beguwa
O
Hystrix cristata
Cricetomys gambianus
Lutra maculicollis
Civetticus civetta
Panthera pardus
Beguwa
Gafiya
Karenruwa
Tunkun juda
Damisa
Felis aurata
Lycaon pictus
Panthera leo
Kawondamisa
Kerkeshi/
Karendaji
Zaki
O
Probably present
R
O
heard (R), scratch
marks (R)
R
R
Crocuta crocuta
Kura
Orycteropus afer
Procavia ruficeps
Potamochoerus porcus
Phacochoerus
africanus
Giant forest hog
Hylochoerus
meinertzhageni
African buffalo
Syncerus caffer
Bushbuck
Tragelaphus scriptus
Red-flanked duiker
Cephalophus rufilatus
Yellow-backed duiker Cephalophus rufilatus
Waterbuck
Kobus ellipsiprymnus
Hartebeest
Alcelaphus
buselaphus
Nile monitor lizard
Varanus niloticus
2
Nile crocodile
Crocodylus niloticus
Many3
Dabganya
Agwada
Jan alde
Alden daji/
Alhanzir
Bakin alde
R (seen at Yakuba,
15 km away)
R (heard at Selbe,
15 km away)
C (burrows)
O
O
O
O
Bauna
Mazo
Makurna
Boka
Gwombaza
Kanki
O
O
O
O
O
O
Guza
Kada
R
R
1
Actual sightings by fieldworkers only; C = common; O = occasional; R = rare.
Not at Kwano but in surrounding area (<20 km distance).
3
More than 431 species identified in GGNP.
2
have two discernible parts: a rapidly declining portion, which reflects the short within-bout
intervals, and a slowly declining portion – the tail of the curve – representing the long between-bout intervals. The bout criterion interval is estimated to be the point at which the
slope changes most rapidly. With this, bouts of chimpanzee acoustic signals can theoretically be discerned.
Nigerian Chimpanzees at Gashaka
Folia Primatol 2004;75:295–316
301
Table 2. Patrols of fieldworkers in the Gashaka-Kwano chimpanzee home
range
Days with
patrols
Days with
opportunistic
records1
Year 2000
January
February
March
April
May
June
July
August
September
October
November
December
Subtotal
7
13
18
0
10
14
8
8
11
5
10
7
111
0
0
1
5
6
8
3
4
0
0
0
0
27
,46
,63
,40
,46
,56
,38
,58
,40
,678
Year 2001
January
February
March
April
May
June
July
August
September
October
November
December
Subtotal
Grand total
8
10
16
26
28
26
21
17
18
27
24
26
247
358
4
0
0
0
4
0
1
2
y1
1
0
2
15
42
,87
,88
,92
,265
,293
,290
,265
,200
,151
,183
,204
,200
2,316
2,994
1
Recording
time, h
,70
,116
,106
Other fieldworkers, labourers, porters.
Each sighting of chimpanzees was treated as an ‘encounter’, defined as lasting from
when the first chimpanzee was visible until the last disappeared. For encounters of only a
few seconds, a minimum length of 1 min was used. At least 3 h had to pass before a new
party count would enter into the analysis. However, in reality, a given party was almost
never found again during a given day once it went out of sight.
The maximum number of chimpanzees visible during an encounter was recorded, as
well as their major activity and the party’s age-sex class composition (adult male, AM; adult
female, AF, with or without swelling; adult of unknown sex; juvenile of either sex; infant of
either sex). It is assumed that the exact number of individuals could be determined in 78% of
the encounters. In the remaining 22%, movements in the vegetation, calls or drumming indicated that more animals were present. In these cases, 1 additional individual was added to
the number of visible animals. All counts were lumped for the analysis.
Following conventions [Mitani et al., 2002], infants were excluded from calculations of
party sizes, but juveniles more or less independent from their mothers were included.
302
Folia Primatol 2004;75:295–316
Sommer/Adanu/Faucher/Fowler
Fig. 4. Home range of the Gashaka-Kwano chimpanzee community as inferred from
acoustic signals (1,705 calls, drumming) and direct sightings (95 encounters) during 2001–
2002. Quadrate distribution not corrected for listening and observation times.
A two-tailed non-parametric Kolmogorov-Smirnov test detected differences between
context-specific samples of party size or encounter length. Correlations were subject to the
Spearman rank correlation test. The level of significance was set at p < 0.05. Given that
sample sizes were often small, we labelled values of p < 0.10 as ‘trend’ and of p < 0.20 as
‘tendency’.
Results
The current analysis is based on 1,705 acoustic signals (calls, drumming) and
95 direct sightings (encounters) of chimpanzees recorded in 2000–2001 (fig. 4).
They occurred in 30 quadrates (grid size 934 m × 934 m) around the Kwano field
station which correspond to 26.2 km2.
Nigerian Chimpanzees at Gashaka
Folia Primatol 2004;75:295–316
303
Fig. 5. Diurnal distribution of acoustic signals (based on 1,577 calls and drumming). Hour
of day: 6 = 6.00–6.59 h, 7 = 7.00–7.59 h, etc.
Fig. 6. Annual distribution of acoustic signals (April 2000 = no data).
304
Folia Primatol 2004;75:295–316
Sommer/Adanu/Faucher/Fowler
Fig. 7. Logarithmic plot of intervals between acoustic signals. WBI = Within-bout
intervals; BBI = between-bout intervals; BCI = bout criterion interval.
Acoustic Signals
Records include 1,481 min in which only vocalizations were heard, 142 min
with vocalizations + drumming and 82 min with only drumming. The proportions
of vocalizations (87%), vocalizations + drumming (8%) and drumming (5%) were
very similar between observation periods, indicating a fair degree of interobserver
reliability (January–December 2000/January–June 2001/July–December 2001: vocalizations 90/87/84%; vocalizations + drumming 5/8/13%; drumming 4/6/4%).
Chimpanzees were seen using feet and one or two hands to produce drum
beats, focusing particularly on buttress roots. The number of beats per drumming,
as recorded during 90 events, was 1 (3.3%), 2 (63.3%) and 3 (33.3%).
Acoustic signals were heard throughout the day with clear peaks in the very
early morning and evening (fig. 5). Chimpanzees call and drum throughout the
year, but monthly rates vary dramatically (fig. 6). There is a tendency towards a
negative correlation with monthly rainfall (rs = –0.301, n = 23, p = 0.163).
We attempted to determine the length of bouts of acoustic signalling by calculating the log survivorship curve for intervals between signals, separately for 3 observation periods and averaged (fig. 7). However, none of the 4 series of cumulative proportions resulted in the expected initial rapid decline of the curve, as exemplified by the following values for the average: up to 1 min 100%, 2 min 91%,
3 min 82%, 4 min 74%, 5 min 67%, 6 min 61%, 7 min 58%, 8 min 55%, 9 min
51%, 10 min 48%,..., 15 min 36%, 20 min 28%,..., 30 min 17%,..., 40 min 12%,...,
50 min 8%,..., 60 min 5%. Thus, the log-transformed plot of these values with their
Nigerian Chimpanzees at Gashaka
Folia Primatol 2004;75:295–316
305
Fig. 8. Party size of Gashaka-Kwano chimpanzees (based on 95 encounters).
rather steady decline did not indicate the expected breaking point between withinbout and between-bout intervals.
Party Size and Composition
Chimpanzees were seen 95 times during 23/24 months. In about half of all
encounters only 1 or 2 individuals were recorded, while the maximum was 17
(fig. 8). The mean across all individual parties was 3.7, and across monthly averages it was 4.1.
Different age/sex classes (AM, AF, juvenile, infant) were recognized to a
varying degree. Individuals were aged a total of 303 times, yielding a party composition of 81% adults, 9% juveniles and 10% infants. To determine the adult sex
ratio, we excluded the many records of encounters with adults of unknown sex.
Sightings in which all adults could be sexed yielded an overall ratio of AM/AF of
0.9 (43/48). This includes cases in which only AM or AF were present as well as
mixed parties with AM and AF. The ratio corresponds well with the figure of 0.8
for mixed parties only (10/13, derived from the combinations AM/AF = 1/1, 1/1,
1/2, 2/2, 1/2, 2/2, 2/3). Unisexual parties were recorded with the following frequencies: 1 AM (n = 5), 2 AM (n = 3); 1 AF (n = 2), 1 AF with 1 infant (n = 5), 1 AF
with 1 juvenile and 1 infant (n = 1), 2 AF with 1 juvenile and 2 infants (n = 1),
3 AF with 2 infants (n = 1).
A fine-tuned analysis revealed that party size was sensitive to methodological,
temporal, spatial and social factors (for the following, see table 3).
Party size had a trend to decline from the first (mean 5.6) to the second year of
study (mean 3.1). Likewise, larger parties (mean 5.4) were significantly more tolerant of observers than smaller ones (mean 2.4). Parties tended to be larger, if infants
306
Folia Primatol 2004;75:295–316
Sommer/Adanu/Faucher/Fowler
Table 3. Correlates of party size and encounter length in Gashaka-Kwano chimpanzees
Party size, n
Encounter length, min
mean SE
median
SD
min. max. n
Overall (years
2000–2001)
3.7
0.4
2
3.5
1
17
95
Year 2000
Year 2001
5.6
3.1
0.9
0.3
4
2
4.6
2.7
1
1
16
17
25
70
test1
+ (p =
0.079)
Enforced as result
of patrol
Opportunistic
Chimpanzees
tolerant
Chimpanzees
nervous/flee
Dry season
(15 Oct–14 Apr)
Wet season
(15 Apr–14 Oct)
mean
SE
median
SD
min. max. n
27
4
10
39
1
190
88
42
22
11
4
30
7
52
33
1
1
190
149
22
66
29
7
4
6
11
1
40
13
1
1
149
30
83
5
45
7
32
44
1
190
39
16
7
1
34
1
149
27
5.4
0.7
4
4.4
1
17
40
2.4
0.4
1.5
2.0
1
7
28
3.6
0.5
3
3.1
1
17
35
40
8
22
49
1
190
34
3.8
0.5
2
3.7
1
16
60
20
4
6
29
1
149
54
73
20
60
61
1
190
9
22
4
7
32
1
149
79
50
18
10
4
35
5
48
31
1
1
190
149
25
63
55
9
32
52
1
190
31
12
2
4
16
1
60
57
Estrous female(s)
present
Estrous female(s)
absent
5.6
1.2
5
3.7
1
14
9
3.5
0.4
2
3.4
1
17
86
Infant(s) present
Infant(s) absent
4.7
3.4
0.8
0.4
3
2
4.3
3.1
1
1
16
17
26
69
Party size below
average
Party size above
average
* (p =
0.046)
+ (p =
0.093)
x (p =
0.141)
Core area of range
Periphery of range2
3.8
3.5
0.5
0.6
2
2.5
3.6
3.0
1
1
17
15
65
30
29
24
6
5
7
13
43
27
1
1
190
103
61
27
Daytime
6.00–8.59 h
9.00–11.59 h
12.00–14.59 h
15.00–17.59+ h
3.7
3.7
3.8
3.4
0.6
0.6
0.9
1.5
3
2
2
2
3.3
3.3
3.7
4.5
1
1
1
1
17
14
16
15
30
32
19
9
33
30
19
17
8
8
7
7
12
11
4
5
43
45
27
20
1
1
1
1
149
190
105
59
30
30
17
9
Travel3
Rest3
Forage3
5.1
4.4
3.4
0.8
1.1
0.5
4
4
3
4.5
4.1
2.4
1
1
1
16
17
9
29
15
25
34
27
33
10
8
7
14.5
20
22
49
30
36
1
1
1
190
95
128
26
15
25
Nest group size
(May 01–Jan 02)4 5.7
0.8
5
5.2
1
23
38
1
Kolmogorov-Smirnov test; * p < 0.05, significant; + = trend (p < 0.10); x = tendency (p < 0.20).
Periphery = outermost quadrates in figure 4 with entries of calls, drumming and/or encounters.
3
Activity at onset of encounter.
4
A. Fowler, unpubl. data.
2
Nigerian Chimpanzees at Gashaka
Folia Primatol 2004;75:295–316
307
test1
x (p =
0.109)
x (p =
0.151)
* (p =
0.017)
x (p =
0.117)
* (p =
0.030)
* (p =
0.014)
* (p =
0.014)
Fig. 9. Annual distribution of party size (August 2000, November 2000 = no data).
were present (mean 4.7) than if infants were absent (mean 3.4), and those including
females with anogenital swellings (mean 5.6) had a tendency to be larger than parties without (mean 3.8). A higher proportion of dry season parties contained swollen females (7/39 = 18%) than wet season parties (2/56 = 4%).
Nevertheless, monthly sizes fluctuated little since 64% of all months had
means of 2–4 (fig. 9). Consequently, party sizes were remarkably similar during the
dry (mean 3.6) and wet seasons (mean 3.8). Similarly, there was no discernible
influence of monthly rain on party size (rs = 0.114, n = 22, p = 0.614) or of monthly
party size on hourly rates of acoustic signals (rs = –0.041, n = 21, p = 0.860).
Party sizes recorded in the core area (mean 3.8) differed also little from those
in the range periphery (mean 3.5). Sizes did likewise not fluctuate much throughout
the day (mean 3.4–3.8) or in relation to activities such as travel (mean 5.1), resting
(mean 4.4) or foraging (mean 3.4).
Encounter Length
Sightings lasted on average 27 min with a maximum of 190 min (for the following, see table 3). Forced encounters – i.e. those, where a patrol team actively
located chimpanzees by e. g. following their calls – lasted on average 29 min. Opportunistic encounters, e.g. by personnel carrying out other research, tended to be
much shorter (mean 7 min). Not surprisingly, tolerated encounters were significantly longer (mean 45 min) than those terminated by flight (mean 17 min). Interestingly, encounters also had a tendency to last longer if more humans were included in a patrol team (1 person = 21 min; 2 = 23 min; 3 = 40 min; 4+ = 28 min;
rs = 0.800, n = 4, p = 0.200).
308
Folia Primatol 2004;75:295–316
Sommer/Adanu/Faucher/Fowler
Fig. 10. Length of encounters as a function of party size.
Fig. 11. The duration and frequency of chimpanzee encounters as a function of cumulative
patrol time.
Nigerian Chimpanzees at Gashaka
Folia Primatol 2004;75:295–316
309
As with party size, numerous other factors influenced encounters. Sightings
tended to be longer during the dry (mean 40 min) than during the wet season
(mean 20 min). Encounters lasted significantly longer if at least 1 infant was present (mean 50 min) compared to parties without infants (mean 18 min). Encounters
with parties that included swollen females (mean 73 min) were also more extended
compared to situations when swollen females were absent (mean 22 min). Moreover, we saw larger than average parties significantly longer (mean 55 min) than
below-average parties (mean 12 min). This is also reflected by the highly significant positive correlation between length of sightings and increasing party size
(fig. 10).
Although encounter length was virtually halved as the day progressed, from
33 min in the mornings to 17 min in the late afternoon, this did not reach statistical
significance. Likewise, there was little difference between parties at travel (mean
34 min), rest (mean 27 min) or foraging (mean 33 min).
Spatial factors also had little influence given the small difference between the
core area (mean 29 min) and the periphery (mean 24 min).
Finally, we assessed if duration and frequency of sightings increased with patrol effort, i.e. whether or not a habituation effect could be detected. There was
clearly no discernible correlation (fig. 11). Somewhat ironically, the longest sighting ever – 190 min – was the very first one, and it almost appeared as if the chimpanzees became less tolerant of observers after about 2,000 h of patrol given the
long period with only relatively short encounters. Also, encounter frequency was
more than double (n = 69) during the first 1,500 h of patrol efforts than during the
second half (n = 26). Similarly, the ratio of tolerated encounters versus those terminated by flight decreased from 3.5 (14/4) in the year 2000 to 1.1 (26/24) in 2001.
Consequently, encounters had a tendency to be twice as long in the first (mean
43 min) compared to the second study year (mean 22 min).
The Kwano Community: Size and Population Density
Chimpanzees were heard or seen and nests were found in about 26.2 km2
around the Kwano field station (fig. 4). Steep and barren hillsides which lead into
open grassland to the west and north, the proximity of Gashaka village in the east,
as well as the relatively broad Ngiti river in the south-east seem to represent
(natural) barriers. Vocal exchanges between chimpanzees were heard across the
banks of the Ngiti river. Thus, the area covered during the present study likely
represents the core of what we believe is inhabited by a single chimpanzee group,
named the ‘Kwano’ community.
We estimated its minimum size via encounters and counts of nest groups [A.
Fowler, unpubl.]. The maximum number of chimpanzees was recorded on January
27, 2001, when a group of schoolchildren and field assistants walking along an
eastern trail were confronted with 17 apes who watched the humans from the
ground and trees over a period of 95 min. Two other nearby patrol teams heard or
saw three other parties estimated to comprise 4, 10 and 4 apes, thus totalling 35
animals.
The largest nest group ever counted was 23 (July 2001). Given that about 20%
of the study population were infants or juveniles who sleep with their mothers, we
arrive at a size of 28 for this nesting party. Assuming that some members slept elsewhere, this supports a minimum community size of 35.
310
Folia Primatol 2004;75:295–316
Sommer/Adanu/Faucher/Fowler
Both the area in which chimpanzees are found as well as the head count is
likely to increase with increasing study time. However, the described barriers in the
range may buffer our figures against underestimates of magnitude. Given that
chimpanzees were sighted in 26 km2, we therefore calculate the population density
as 1.3 apes/km2.
Discussion
Our study is the first to provide detailed eco-ethological information for the
newly recognized chimpanzee subspecies P. t. vellerosus from what might be the
only viable population.
Vegetation and climate at Gashaka (fig. 2) is similar to mixed-vegetation Tanzanian sites (Gombe: 1,775 mm rain during 152 days, mean max. temp. 28°C, mean
min. temp. 19°C; Mahale: 1,836 mm rain during 141 rainy days, mean max. temp.
27°C, mean min. temp. 19°C). The climate thus occupies a middle position between
very dry (Assirik/Senegal: 954 mm rain) and wet sites (Boussou/Guinea: 2,230 mm
[Hunt and McGrew, 2002]). Gashaka has a larger set of predators (leopard, lion,
hyaena, wild dog) compared to most other chimpanzee study sites. The area therefore represents the West African equivalent of a chimpanzee site similar to the hypothesized forest-woodland habitat in which early humans lived [Hunt and
McGrew, 2002].
Acoustic Signals
At new sites – such as Gashaka – researchers rely on acoustic signals
[Goodall, 1986] to locate the apes [Hunt and McGrew, 2002]. Chimpanzees vocally
express emotions and convey information, e.g. about food sources and danger.
Drumming against tree buttresses – the most prominent non-vocal sound signal –
earned Nigerian chimpanzees the Hausa name ‘biri mai ganga’ (‘monkey with the
drum’).
Loud calls, particularly pant-hoots, are often given when parties meet during
nesting and at the beginning of the day [Goodall, 1986; Hunt and McGrew, 2002].
The evening peak (fig. 5) might therefore reflect the joining of smaller day parties
(mean 3.7) for night nest groups (mean 5.7). The early morning peak seems to reflect decisions about party composition and travel directions.
Calls and drumming tended to decrease with increasing rainfall. Denser vegetation which muffles sounds as well as observer fatigue may have led to underreporting during rains, particularly because party sizes hardly differed between the
dry and wet season (table 3) and because rates of acoustic signals did not correlate
with party size.
We were unable to assess the expected breaking point between within-bout
and between-bout intervals of acoustic signalling because the log-transformed
graph declined monotonously (fig. 7). This is probably because we could not normally distinguish signals from different parties – i.e. discern intra-party and distance signals – particularly when heard from afar. Thus, the signal from a second
party would often fill in and mask the between-bout interval of a first party. As a
result, we are unable to determine a bout criterion interval. Short of being able to
identify individual callers [Boesch and Boesch-Achermann, 2000], observers would
Nigerian Chimpanzees at Gashaka
Folia Primatol 2004;75:295–316
311
have to travel continuously with the chimpanzees to at least reliably record the signals of individual parties.
Party Size
Overall party size varied greatly with, however, a skew toward the right
(fig. 8). Consequently, the median (2) was smaller than the mean (3.7) – a result in
line with other studies [Mitani et al., 2002]. The average of the monthly mean party
sizes was greater (4.1) and nest group size even larger (mean 5.7). Thus, comparisons with other sites are problematic, particularly since methodological, ecological,
social and spatial factors cause further fluctuations (see below).
Nevertheless, it is known that the smaller the community, the larger the relative party size (i.e. mean party size/community size × 100 [Boesch and BoeschAchermann, 2000]). If we assume a size of 35 for the Gashaka-Kwano community,
party sizes of 3.7, 4.1 and 5.7 translate into relative sizes of 11, 12 and 16%, respectively. These values are well within the observed cross-population range and
e.g. close to Budongo/Uganda (12%) or Taï/Ivory Coast (13%). Thus, our data
might confirm that smaller communities are socially less fluid, indicating that not
only food competition influences fission-fusion, but perhaps also predation pressure
[Boesch and Boesch-Achermann, 2000], which could be considerable at Gashaka
(table 1).
Our data on party composition are scarce since many parties had unknown
composition (see Lanjouw [2002] for a similar problem). The overall socionomic
sex ratio (AM/AF = 0.90) is within the variation at other sites [Boesch et al., 2002].
However, juveniles and infants at Gashaka make up only 19% of the community,
half the proportion for e.g. Kanyawara/Uganda (63% adults, 13% juveniles, 24%
infants [Wrangham, 2002]). Probably, as elsewhere during initial study years (e.g.,
Taï/Ivory Coast [Boesch and Boesch-Achermann, 2000]), lactating females were
particularly wary of observers, leading to underreporting. Indeed, females with
infants tended to be found in larger than average parties which were more tolerant
of humans (table 3). Potential underreporting not withstanding, lactating females
still represent the highest proportion of unisexual parties at Gashaka, perhaps because scramble competition restricts their travel and sociability (see Williams et al.
[2002] for Gombe/Tanzania).
Party size had a trend to increase when estrous females were present, and encounters lasted significantly longer (table 3), in line with many other reports
[Hashimoto et al., 2001; Anderson et al., 2002; Matsumoto-Oda, 2002; Mitani et
al., 2002; Wrangham, 2002; Wallis, 2002]. It is typically hypothesized that party
sizes increase because males seek sexually receptive females or because such females seek copulations [Wallis, 2002; Wrangham, 2002]. A tendency for cycle onset during the dry season is reported from Budongo/Uganda and Gombe/Tanzania,
probably as a result of feeding conditions which stimulate hormonal activities
[Wallis, 2002]. The Gashaka data support this, since 18% of dry season parties but
only 4% of wet season parties contained swollen females.
Mean party size, however, did not differ between the wet and dry seasons
(table 3), and monthly rainfall and party size were not correlated. It is often assumed that rain stimulates plant productivity so that rain can be used as a proxy for
food availability (review in Mitani et al. [2002]). Nevertheless, while the dry season may correspond to food scarcity (Taï/Ivory Coast [Doran, 1997]), this is not
312
Folia Primatol 2004;75:295–316
Sommer/Adanu/Faucher/Fowler
necessarily the case (e.g. Mitani et al. [2002] for Ngogo/Uganda). Moreover, party
size may increase with fruit abundance at some sites [Mitani et al., 2002] but not at
others (Kalinzu/Uganda) [Hashimoto et al., 2001].
We were unable to replicate findings for Taï/Ivory Coast [Anderson et al.,
2002] that parties were smaller (a) while travelling, (b) during mid-day and (c) in
the range core where aggressive territorial encounters are less likely (table 3). Admittedly, our data are of lower quality. On the other hand, the Gashaka-Kwano
community might have immediate neighbours only in the south-west of their range
where the forest is continuous. Here, a hostile interaction between males was indeed observed during 2002 [A. Fowler, pers. observation].
Encounter Length
Various socio-ecological and methodological factors influenced the durations
of chimpanzee sightings (table 3).
For example, opportunistic encounters tended to be shorter than those resulting
from dedicated patrols, most likely because opportunistic observers had no particular reason to stay with or follow the chimpanzees they had encountered by chance.
Somewhat surprisingly, encounters were extended if observation teams were larger.
Chimpanzees will at times watch travellers on the footpath from trees in the vicinity. Thus, relatively noisy groups of humans are probably associated with less danger than single observers who may be perceived as trying to furtively approach.
Clearly, encounter length depended on how relaxed the chimpanzees remained.
Flight was particularly likely if observers came across chimpanzees unexpectedly
and thus without warning.
Sightings tended to be shorter during the rains, perhaps because it is much
more difficult to see or follow chimpanzees in dense and wet vegetation, often with
heavy downpours. Moreover, due to reduced visibility, observers can inadvertedly
startle chimpanzees, causing them to flee.
Encounters lasted significantly longer if parties contained infants or swollen
females. Such parties were also larger, which seems to increase tolerance to observers since encounters with larger than average parties lasted significantly longer and
the length of sightings increased with party size (fig. 10).
Habituation Efforts
Chimpanzees at Gashaka are not extremely wary towards observers because
they are used to see humans walking on foot through their habitat. Nevertheless,
party size had a trend to be smaller during our second study year (table 3). One
might conclude that the chimpanzees became less tolerant of researchers. However,
it is also possible that smaller parties later on in the study allowed observers to approach more often. In addition, observers probably became increasingly better in
tracking down smaller groups which are harder to locate.
Similarly, both frequency and length of encounters decreased markedly over 2
years (fig. 11, table 3). However, instead of concluding that our research did ‘dehabituate’ the chimpanzees, one has to consider that, over the course of the study,
observers patrolled wider and wider areas in more rugged terrain. Consequently,
the success of seeing and remaining with chimpanzees decreased. Finally, chimpanzees regularly passed through camp in the beginning of the study but ceased doing
so later on, similar to bonobos at Lomako/DRC [G. Hohmann, pers. commun.].
Nigerian Chimpanzees at Gashaka
Folia Primatol 2004;75:295–316
313
On average, a single sighting was achieved after 31.5 h (2.6 days). Assuming a
community size of at least 35 and a mean party size (including infants) of 4.0 individuals, it takes 8.8 sightings until all members encounter an observer. Thus, the
average interval between the sightings of an individual chimpanzee is currently
22.8 days.
Clearly, we will have to improve rates of sightings and increase the degree of
habituation. Only a fraction of the large home range could be monitored during a
given day. Chimpanzee calls do not travel across several hillsides that dissect the
range and we did therefore sometimes not hear calls for several successive days.
Moreover, patrols could not alert each other to the presence of chimpanzees since
hand-held radios did not carry signals across hilltops either.
A recently erected transmitter station does now allow us to place radioequipped patrols on elevated observation points who report calls back to the field
station. Researchers then target specific segments of the home range instead of conducting more or less random searches. We are confident that this strategy will increase the rate and duration of chimpanzee sightings considerably.
Population Density
Our research indicates that the Gashaka-Kwano chimpanzee community comprises at least 35 members ranging over at least 26 km2 which translates into a
population density of 1.3 apes/km2. If these are close to the actual figures, then the
Gashaka chimpanzees would have a relatively small community in a relatively
large range, compared to Tanzanian chimpanzees which live in similar climate and
habitat: Gombe, 40–45 animals (Kasakela), range 4–24 km2; Mahale, 83 animals
(M group), 7–14 km2 [Hunt and McGrew, 2002]. However, while our data are preliminary, it is conceivable that food supplies are more scarce at Gashaka.
Previous census work in Gashaka Gumti National Park generated variable figures for chimpanzees per square kilometre (Dunn [1993]: 1.1; Hogarth [1997]:
0.75; Foster [1998]: 0.24–1.12; Adanu [1998]: 0.2–2.1; Lameed [2002]: 2.02). The
divergence reflects different techniques of nest-counting (straight line vs. nonrandom transects) and surveyed habitats (lowland forest, mountainous forest,
woodland). These densities translate to a total of 900–1,700 weaned chimpanzees in
GGNP. Such figures depend on assessments of suitable habitat within the park.
This is a difficult task, given the mosaic nature of plant cover and lack of updated
vegetation maps based on remote sensing. Nevertheless, GGNP and the GashakaKwano area in particular are certainly premier sites which could ensure the survival
of P. t. vellerosus in the wild.
Outlook
Forthcoming publications will focus on the plant composition of the Kwano
forests, feeding ecology, nesting pattern and material culture of the GashakaKwano chimpanzees (tools, potential use of medicinal plants [McGrew, 1992;
Huffmann, 1997]). Detailed behavioural studies have to rely on more direct observations, but we are hopeful that the degree of chimpanzee habituation will increase
in the future.
Long-term research at Gashaka will improve the understanding of the ecological and cultural flexibility of chimpanzees [McGrew et al., 1996; Whiten et al.,
1999], given that very little is known about P. t. vellerosus. Moreover, studies at a
314
Folia Primatol 2004;75:295–316
Sommer/Adanu/Faucher/Fowler
West African mosaic chimpanzee habitat should broaden our knowledge about the
conditions under which Mio-Pliocene hominids lived [Hunt and McGrew, 2002].
Acknowledgment
The Nigeria National Park Service kindly granted a research permit to the Gashaka
Primate Project. Particularly helpful in the development of the project was the advice of
Andrew Dunn and Richard Barnwell. Gashaka Gumti National Park, the Nigerian Conservation Foundation and WWF-UK provided vital logistical support. The fieldwork was sponsored by generous conservation grants from the North of England Zoological Society/
Chester Zoo, as well as by the Leakey Foundation/San Francisco and Leventis Ltd. & ProNatura International/Lagos. Additional support came from the Leakey Fund/London (to
A.F.), the Dean’s Travel fund of UCL (to V.S.) and Primate Conservation Inc. (to J.A.).
Claire Bracebridge, Julia Greenslade, Asako Saegusa, Judith Bovensiepen, Jennifer Rogan,
Maurice Melle Ekane, Ymke Warren, Umaru Buba and Yakubu Wakirwa volunteered in
data collection. The work would have been impossible without local field assistants, in particular Hammaunde Guruza, Salamu Waziri, Buba Bello, Bobbo Buba and Ali Tappare. We
thank William McGrew and two anonymous reviewers for helpful comments.
References
Adanu J (1997). Determination of Life-Span of Chimpanzee Nests (Nest-Aging) in Gashaka-Gumti
National Park. Project report. Gashaka, Nigerian Conservation Foundation/WWF-UK.
Adanu J (1998). Distribution and Abundance of Chimpanzees (Pan troglodytes) in Gashaka Gumti
National Park, Nigeria. UG dissertation, Yola.
Anderson DP, Nordheim EV, Boesch C, Moermond TC (2002). Factors influencing fission-fusion
grouping in chimpanzees in the Taï National Park, Côte d’Ivoire. In Behavioural Diversity in
Chimpanzees and Bonobos (Boesch C, Hohmann G, Marchant LF, eds.), pp 90–101. Cambridge,
Cambridge University Press.
Boesch C, Boesch-Achermann H (2000). The Chimpanzees of the Taï Forest: Behavioural Ecology and
Evolution. Oxford, Oxford University Press.
Boesch C, Hohmann G, Marchant LF (eds.) (2002). Behavioural Diversity in Chimpanzees and Bonobos. Cambridge, Cambridge University Press.
Chapman JD, Chapman HM (2001). The Forests of Taraba and Adamawa States, Nigeria: An Ecological Account and Plant Species Checklist. Canterbury, University of Canterbury/NZ, WWF/DFID.
Doran D (1997). Influence of seasonality on activity patterns, feeding behaviour, ranging and grouping
patterns in Taï chimpanzees. International Journal of Primatology 8: 18–206.
Dunn A (1993). The Large Mammals of Gashaka-Gumti National Park, Nigeria: Line Transect Surveys
from Forest and Savannah. Project report. Gashaka, Federal Ministry of Agriculture, Nigeria,
Nigerian Conservation Foundation/WWF-UK.
Dunn A (1999). Gashaka Gumti National Park: A Guidebook. Lagos, Gashaka Gumti National Park,
NCF/WWF-UK.
Foster KL (1998). Censusing Chimpanzees in Gashaka-Gumti National Park, Taraba and Adamawa
States, Nigeria. Project report. Gashaka, Federal Ministry of Agriculture, Water Resources and
Rural Development, Nigeria, Nigerian Conservation Foundation/WWF-UK.
Gonder K, Oates J, Disotell T, Forstner M, Morales J, Melnick D (1997). A new West African chimpanzee subspecies? Nature 388: 337.
Goodall J (1986). The Chimpanzees of Gombe: Patterns of Behaviour. Cambridge, Harvard University
Press.
Harcourt CS, Ellerton NG (1995). A Brief Look at the Primates of Gashaka-Gumti National Park, Nigeria. Project report. Gashaka, Nigerian Conservation Foundation/WWF-UK.
Hashimoto C, Furuichi T, Tashiro Y (2001). What factors affect the size of chimpanzee parties in the
Kalinzu forest, Uganda? Examination of fruit abundance and number of estrous females. International Journal of Primatology 22: 947–959.
Hogarth SA (1997). The Distribution and Abundance of the Chimpanzees (Pan troglodytes) of the Lowland Gallery Forest of Gashaka-Gumti National Park, Nigeria. Project report. Gashaka, Federal
Ministry of Agriculture, Water Resources and Rural Development, Nigeria, Nigerian Conservation Foundation/WWF-UK.
Nigerian Chimpanzees at Gashaka
Folia Primatol 2004;75:295–316
315
Huffman MA (1997). Current evidence for self-medication in primates: A multidisciplinary perspective.
Yearbook of Physical Anthropology 40: 171–200.
Hunt KD, McGrew WC (2002). Chimpanzees in the dry habitats of Assirik, Senegal and Semliki Wildlife Reserve, Uganda. In Behavioural Diversity in Chimpanzees and Bonobos (Boesch C, Hohmann G, Marchant LF, eds.), pp 35–51. Cambridge, Cambridge University Press.
Lameed GA (2002). Chimpanzee (Pan troglodytes) population density and structure in Gashaka Gumti
National Park. ROAN, The Journal of Conservation 1: 88–93.
Lanjouw A (2002). Behavioural adaptations to water scarcity in Tongo chimpanzees. In Behavioural
Diversity in Chimpanzees and Bonobos (Boesch C, Hohmann G, Marchant LF, eds.), pp 52–60.
Cambridge, Cambridge University Press.
Louppe D, Oattara N, Coulibaly A (1995). The effects of brush fires on vegetation: The Audrville fire
plots after 60 years. Commonwealth Forestry Review 74: 288–292.
McGrew WC (1992). Chimpanzee Material Culture: Implications for Human Evolution. Cambridge,
Cambridge University Press.
McGrew WC, Marchant LF, Nishida T (eds) (1996). Great Ape Societies. New York, Cambridge University Press.
Manson JH, Wrangham RW (1991). Intergroup aggression in chimpanzees and humans. Current Anthropology 32: 369–390.
Martin P, Bateson P (1986). Measuring Behaviour. Cambridge, University of Cambridge Press.
Matsumoto-Oda A (2002). Social relationships between cycling females and adult males in Mahale
chimpanzees. In Behavioural Diversity in Chimpanzees and Bonobos (Boesch C, Hohmann G,
Marchant LF, eds.), pp 168–180. Cambridge, Cambridge University Press.
Mitani J, Watts DP, Lwanga JS (2002). Ecological and social correlates of chimpanzee party size and
composition. In Behavioural Diversity in Chimpanzees and Bonobos (Boesch C, Hohmann G,
Marchant LF, eds), pp 102–112. Cambridge, Cambridge University Press.
Moore J (1996). Savanna chimpanzees, referential models and the last common ancestor. In Great Ape
Societies (McGrew WC, Marchant LF, Nishida T, eds.), pp 275–292. New York, Cambridge
University Press.
Pearce J, Ammann K (1995). Slaughter of the Apes: How the Tropical Timber Industry Is Devouring
Africa’s Great Apes. London, World Society for the Protection of Animals.
Sommer V, Ammann K (1998). Die Grossen Menschenaffen: Orang-utan, Gorilla, Schimpanse, Bonobo. Munich, BLV.
Wallis J (2002). Seasonal aspects of reproduction and sexual behavior in two chimpanzee populations:
A comparison of Gombe (Tanzania) and Budongo (Uganda). In Behavioural Diversity in Chimpanzees and Bonobos (Boesch C, Hohmann G, Marchant LF, eds.), pp 181–191. Cambridge,
Cambridge University Press.
Whiten A, Goodall J, McGrew WC, Nishida T, Reynolds V, Sugiyama Y, Tutin CEG, Wrangham RW,
Boesch C (1999). Cultures in chimpanzees. Nature 399: 682–685.
Williams JM, Liu H-Y, Pusey AE (2002). Costs and benefits of grouping for female chimpanzees at
Gombe. In Behavioural Diversity in Chimpanzees and Bonobos (Boesch C, Hohmann G, Marchant LF, eds.), pp 192–203. Cambridge, Cambridge University Press.
Wrangham R (2002). The costs of sexual attraction: Is there a trade-off in female Pan between sex
appeal and receiving coercion? In Behavioural Diversity in Chimpanzees and Bonobos (Boesch C,
Hohmann G, Marchant LF, eds.), pp 204–215. Cambridge, Cambridge University Press.
Wrangham RW, McGrew WC, de Waal FBM, Heltne PG (eds.) (1994). Chimpanzee Cultures. Cambridge, Harvard University Press.
316
Folia Primatol 2004;75:295–316
Sommer/Adanu/Faucher/Fowler